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Sensorimotor Hallucinations in Parkinson's Disease

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Sensorimotor Hallucinations in Parkinson's Disease Supplementary Information Sensorimotor hallucinations in Parkinson’s disease Fosco Bernasconi*1, Eva Blondiaux*1, Jevita Potheegadoo1, Giedre Stripeikyte1, Javier Pagonabarraga2,3,4,5, Helena Bejr-Kasem2,3,4,5, Michela Bassolino1, Michel Akselrod1,6, Saul Martinez-Horta2,3,4,5, Fred Sampedro2,3,4,5, Masayuki Hara9, Judit Horvath7, Matteo Franza1, Stéphanie Konik1,6, Matthieu Bereau7,8, Joseph-André Ghika10, Pierre R. Burkhard7, Dimitri Van De Ville12,13, Nathan Faivre1,11, Giulio Rognini1, Paul Krack14, Jaime Kulisevsky2,3,4,5, and Olaf Blanke1,7 Affiliations 1. Laboratory of Cognitive Neuroscience, Center for Neuroprosthetics & Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne (EPFL), Geneva, Switzerland 2. Movement Disorders Unit, Neurology Department Sant Pau Hospital, Barcelona, Spain 3. Universitat Autònoma de Barcelona (UAB), Spain 4. Centro de Investigación en Red-Enfermedades Neurodegenerativas (CIBERNED), Spain 5. Biomedical Research Institute (IIB-Sant Pau), Barcelona, Spain 6. University Hospital of Lausanne, CHUV, Lausanne, Switzerland 7. Department of Neurology, Geneva University Hospitals, Geneva, Switzerland 8. Department of Neurology, Besançon University Hospital, Besançon, France 9. Graduate School of Science and Engineering, Saitama University, Japan 10. Department of Neurology, Hôpital du Valais, Sion, Switzerland. 11. Laboratoire de Psychologie et Neurocognition, LPNC, CNRS 5105 Université Grenoble Alpes, France 12. Medical Image Processing Laboratory, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland 13. Department of Radiology and Medical Informatics, University of Geneva, Geneva, Switzerland 14. Department of Neurology, Inselspital, University Hospital and University of Bern, Bern, Switzerland. 1 Authors’ contributions FB designed Study 1 and 3, collected & analyzed data, conducted clinical interviews, wrote paper; EB designed Study 2, collected & analyzed data, wrote paper; J. Potheegadoo collected data, designed questionnaire for semi-structured interview, conducted clinical interviews and clinical evaluations for study 1; GS analyzed data for study 3; J. Pagonabarraga, HB and JK recruited patients, conducted clinical interviews, collected data for study 3; MA and NF analyzed data for study 2; MB collected data, conducted clinical interviews and clinical evaluations for study 1; MF collected data for study 1; SK coordinated the recruitment for study 1; SMH designed and conducted clinical interviews for study 3; FS collected data for study 3; MH designed and developed the robotic systems; JH, JG, PB recruited patients and conducted clinical evaluations for study 1; DV designed study 2; PK designed study 1; GR and OB designed study 1, 2 and 3, wrote paper. All authors provided critical revisions and approved the final version of the paper for submission. All the authors declare no competing interests. Acknowledgments We thank Dr. Didier Genoud and Dr. Vanessa Fleury for their contribution in recruiting patients. * These authors equally contributed to the work Co-corresponding authors Olaf Blanke Bertarelli Chair in Cognitive Neuroprosthetics Center for Neuroprosthetics & Brain Mind Institute School of Life Sciences Campus Biotech Swiss Federal Institute of Technology Ecole Polytechnique Fédérale de Lausanne (EPFL) CH – 1012 Geneva E-mail: [email protected] Tel: +41 (0)21 693 69 21 Jaime Kulisevsky Movement Disorders Unit Neurology Department Hospital de la Santa Creu i Sant Pau Mas Casanovas 90, 08041 Barcelona, Spain E-mail address: [email protected] 2 Funding: Carigest SA, Swiss National Science Foundation (3100A0-112493), Parkinson Suisse, Bertarelli Foundation to Olaf Blanke, CIBERNED (Carlos III Institute) to Jaime Kulisevsky, JSPS Fund for the Promotion of Joint International Research (Fostering Joint International Research) (17KK0003) to Masayuki Hara. Keywords: Parkinson’s disease, Hallucinations, Sensorimotor, fMRI, cognitive decline Study 1 Study 1.1: Robot-induced presence hallucinations (riPH) in patients with PD Supplementary S1 Participants: Inclusion/Exclusion criteria Participants in the present study consisted of patients with PD and the symptom of PH (PD-PH, n=13), patients with PD without the symptom of PH (PD-nPH, n=13), and age-matched healthy controls (HC, n=21). Demographic and clinical data are summarized in Table S1. Patients with cognitive impairments (defined as a MoCA score1 lower then 242), treated with neuroleptics, affected by other central neurological co-morbidities, affected by psychiatric co-morbidities unrelated to PD, and patients with recent (< one month) changes in their medical treatment were not included in the study. The HC included in the study never experienced PH, did not suffer from a neurological or psychiatric disease, and had no objective sign of cognitive impairment. Supplementary S2 Demographic and disease-related variables For every PD patient, the doses of anti-parkinsonian medication were converted to the levodopa equivalent daily dose3. The severity of motor symptoms was assessed by the score at the Movement Disorders Society - Unified Parkinson Disease Rating Scale (MDS-UPDRS) - part III (Goetz et al., 2008), in “ON” state. In addition, impulsive-compulsive disorders were assessed by the score at the “Questionnaire for Impulsive-Compulsive Disorders in Parkinson’s Disease” (QUIP-RS4). We also assessed for PD-PH, PD-nPH, and HC apathy scale5 and the risk for psychosis 3 (Prodromal Questionnaire PQ-166; which was divided in part I (hallucinations, and negative symptoms-like experiences), and part II (level of distress linked to the experiences). Hallucinations were assessed with a semi-structured interview adapted from the psychosensory hallucinations Scale (PSAS) for Schizophrenia and Parkinson’s disease7. Next to PH, we also inquired about other hallucinations possibly experienced by patients with PD, e.g. passage hallucinations (i.e., animal, person or indefinite object passing in the peripheral visual field), visual illusion and complex hallucinations (structured visual, auditory or tactile hallucinations) as well as delusional ideas. PD-PH (N = 13) PD-nPH (N = 13) p-values Age 60.69 ± 13.19 65.69 ± 7.60 0.25 Gender 9 (M) 4 (M) 0.05 (χ2) UPDRS-III 20 ± 12.09 19 ± 17.51 0.87 MoCA 26.85 ± 1.82 28.15 ± 1.57 0.08 PQ16 4.00 ± 2.00 0.69 ± 1.32 < 0.001 PQ16-2 3.54 ± 4.86 1.08 ± 2.63 0.1 Apathy 12.69 ± 8.06 10.23 ± 4.64 0.37 LEDD (mg/day) 727.77 ± 410.46 786.23 ± 657.23 0.8 Disease Duration (years) 9.46 ± 4.22 9.38 ± 5.72 0.5 Table S1. Clinical variables between PD-PH and PD-nPH. PD-PH (N = 13) HC (N = 21) p-values Age 60.69 ± 13.19 66.90 ± 5.75 0.06 Gender 9 (M) 11 (M) 0.9 (χ2) MoCA 26.85 ± 1.82 28.52 ± 1.03 <0.001 PQ16 4.00 ± 2.00 0.24 ± 0.44 <0.001 PQ16-2 3.54 ± 4.86 0 ± 0 <0.001 Apathy 12.69 ± 8.06 6.33 ± 4.05 0.01 Table S2. Clinical variables between PD-PH and HC. 4 Supplementary S3 Experimental procedure Each PD patient underwent study1 at a similar time (10am), after having received their usual anti-parkinsonian medication and were in their “best ON” state for the whole duration of study1 as well as the psychological and neuropsychological assessments8. To investigate the riPH in patients with PD (and HC), we used the same experimental setup and device as our previous research9. The robotic stimulation was administered through a robotic system10 that has previously been used to induce the PH and other bodily illusions in healthy subjects9. The experimental design consisted in factors Synchrony (synchronous/asynchronous), Side (most/less affected) and Group (PD-PH/PD-nPH). Supplementary S4 Questionnaire results: PH Detailed ratings for all questions can be seen on Table S3 (below). riPH (“I felt as if someone was close-by”) PD-PH vs. PD-nPH. No main effect of Side (permutation p-value=0.37). No interactions were observed, all permutation p-values>0.05. PD-PH vs. HC. By comparing PD-PH and HC, we confirmed the importance of conflicting sensorimotor stimulation to induced PH, as both groups gave higher PH ratings in the asynchronous versus synchronous condition (p-value=0.033). The intensity of riPH ratings did not differ statistically between PD-PH and HC (permutation p-value=0.48). The Side did not significantly modulate the riPH ratings (permutation p-value=0.38). No interactions were observed, all permutation p-values>0.05. Supplementary S5 Questionnaire results: Other robot-induced perceptions Passivity experience (“I felt as if someone else was touching my back.”). 5 PD-PH vs. PD-nPH. The two sub-groups of patients did not report difference in passivity experiences in the asynchronous condition (permutation p-value = 0.1, main effect of Synchrony), the ratings did not differ significantly between the groups of patients (permutation p-value = 0.38, main effect of Group), and the Side did not modulate the passivity experience (permutation p-value=0.41). No interactions were observed, all permutation p-values>0.05. PD-PH vs. HC. We observed a trend for asynchronous condition to induce higher passivity experiences in the asynchronous condition (permutation p-value=0.06, main effect of Synchrony). The ratings were not statistically different between the groups (permutation p-value=0.86, main effect of Group). The Side modulated the passivity experience (permutation p-value<0.01). No interactions were observed, all other permutation p-values>0.05. Self-touch (“I felt as if I was touching my back.”). PD-PH vs. PD-nPH. In line with previous work9, the two sub-groups of patients reported higher self-touch experiences in the synchronous condition (permutation p-value=0.043, main effect of Synchrony). The ratings did not differ significantly neither between the groups of patients (permutation p-value=0.65, main effect of Group), nor between the Side (permutation p-value=0.51). No interactions were observed, all other permutation p-values>0.05. PD-PH vs. HC. We observed that participants reported a trend for higher self-touch experiences in the synchronous condition (permutation p-value=0.054, main effect of Synchrony).
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